Elsevier

Chemosphere

Volume 75, Issue 6, May 2009, Pages 745-750
Chemosphere

Biodegradation of endocrine-disrupting compounds and suppression of estrogenic activity by ligninolytic fungi

https://doi.org/10.1016/j.chemosphere.2009.01.034Get rights and content

Abstract

Endocrine-disrupting compounds (EDCs) represent a large group of substances of natural and anthropogenic origin. They are widely distributed in the environment and can pose serious risks to aquatic organisms and to public health. In this study, 4-n-nonylphenol, technical 4-nonylphenol, bisphenol A, 17α-ethinylestradiol, and triclosan were biodegraded by eight ligninolytic fungal strains (Irpex lacteus 617/93, Bjerkandera adusta 606/93, Phanerochaete chrysosporium ME 446, Phanerochaete magnoliae CCBAS 134/I, Pleurotus ostreatus 3004 CCBAS 278, Trametes versicolor 167/93, Pycnoporus cinnabarinus CCBAS 595, Dichomitus squalens CCBAS 750). The results show that under the used conditions the fungi were able to degrade the EDCs within 14 d of cultivation with exception of B. adusta and P. chrysosporium in the case of triclosane and bisphenol A, respectively. I. lacteus and P. ostreatus were found to be most efficient EDC degraders with their degradation efficiency exceeding 90% or 80%, respectively, in 7 d. Both fungi degraded technical 4-nonylphenol, bisphenol-A, and 17α-ethinylestradiol below the detection limit within first 3 d of cultivation. In general, estrogenic activities assayed with a recombinant yeast test decreased with advanced degradation. However, in case of I. lacteus, P. ostreatus, and P. chrysosporium the yeast assay showed a residual estrogenic activity (28-85% of initial) in 17α-ethinylestradiol cultures. Estrogenic activity in B. adusta cultures temporally increased during degradation of technical 4-nonylphenol, suggesting a production of endocrine-active intermediates. Attention was paid also to the effects of EDCs on the ligninolytic enzyme activities of the different fungi strains to evaluate their possible stimulation or suppression of activities during the biodegradation processes.

Introduction

Endocrine-disrupting compounds (EDCs) are a group of environmental pollutants known for their negative influence, particularly on aquatic organisms. Several studies demonstrated that these chemicals mimic hormones or interfere with the action of endogenous hormones (White et al., 1994, Ishibashi et al., 2004). Due to their widespread presence in the environment and toxic activity even at low concentrations, EDCs have received increased attention in water quality management and health care.

Typical EDCs of anthropogenic origin with estrogen-like action include 4-nonylphenols (NPs), bisphenol A (BPA), and 17α-ethinylestradiol (EE2). Mimicking natural hormones or disruption of biosignal pathways by these chemicals can stimulate the growth of human breast cancer cells (Soto et al., 1991) or induce the expression of vitellogenin in fish (Kwak et al., 2001). As a consequence, both mechanisms are used to prove estrogen activity by bioassays. NPs mainly occur in the environment as degradation products of nonylphenolpolyethoxylates, which are used widely as non-ionic surfactants in many industrial applications. Due to their hydrophobic properties, these compounds are considered to be slowly biodegraded under aerobic conditions (Ying et al., 2002). BPA is a raw material of some polycarbonates and epoxy resins and it is widespread used as food packaging material (Biles et al., 1997). Moreover, the compound leaches also from dental materials and it was also found in waste landfill leachates (Yamamoto et al., 2001).

Synthetic estrogens, such as EE2, are used as oral contraceptives. Non-metabolized EE2 and its conjugates are excreted into wastewater. During sewage treatment, EE2 is then released from the corresponding conjugates by hydrolysis and reaches the environment via the effluents of wastewater treatment plants (Tyler and Routledge, 1998). Due to their incomplete removal during the waste treatment process, synthetic and natural estrogens are considered as major contributors to the estrogenic activity associated with waste water treatment plant effluents (Gutendorf and Westendorf, 2001).

Among the EDCs present in the environment, increasing interest is being given to antibiotics suspected of creating multiresistant germs. Triclosan (TRC) is an established bacteriostatic compound and widely used as fungicide in topical and dental preparations. It is known to be absorbed in the gastrointestinal tract and through the skin (Dayan, 2006).

EDCs tend to accumulate in aquatic organisms and to be adsorbed by sediments and on particles in the aquatic environment (Adolfsson-Erici et al., 2002). The role that the mixture of bacteriocides and EDCs plays in the environment is currently not well understood. Due to their high bioactivity, ubiquitous nature, toxicity and persistence, it is of extreme importance to investigate and study organisms that have the ability to reduce these substances in the environment. A promising way to do so is the application of ligninolytic fungi or isolated fungal enzymes for the biodegradation of these compounds.

Ligninolytic fungi produce extracellular enzymes with low substrate specificity, which makes them suitable for degradation of various aromatic compounds, even with low water solubility. Their advantage in many cases over bacteria is attributed to the extracellular nature of the ligninolytic enzymes. In addition, they secrete low molecular weight mediators that enlarge the spectrum of compounds they are able to oxidize (Pointing, 2001). The ligninolytic system consists of four major enzymes: lignin peroxidase (LiP, E.C. 1.11.1.14), manganese-dependent peroxidases (MnP, E.C. 1.11.1.13), versatile peroxidases (VP, E.C. 1.11.1.16) and laccases (Lac, E.C. 1.10.3.2). In vivo and in vitro experiments with purified enzymes proved that ligninolytic enzymes were able to extensively degrade EDCs (Tanaka and Taniguchi, 2003, Keum and Li, 2004, Corvini et al., 2006, Cabana et al., 2007a, Cabana et al., 2007b, Shin et al., 2007). On the other hand, there are not many studies comparing degradation abilities of different strains of ligninolytic fungi on EDCs. It was also shown that presence of aromatic pollutants can influence production of the enzyme activities in fungal cultures (Cajthaml et al., 2008). Moreover, only a few authors monitored changes in the endocrine-disrupting activity during the fungal biodegradation (Cabana et al., 2007b).

The aim of this paper is to investigate abilities of whole cultures of eight ligninolytic fungal strains to degrade several typical representatives of EDCs and to evaluate changes in the estrogenic activity of the samples. Attention was also paid to the effect of EDCs on ligninolytic enzyme activities in order to evaluate a possible stimulation or suppression of the activities.

Section snippets

Chemicals

Technical nonylphenol mixture (ring and chain isomers) and 4-n-nonylphenol (4-n-NP, ⩾98%), BPA (⩾99%), EE2 (⩾98%), and TRC (⩾97.0%) were used as substrates for degradation experiments and were purchased from Aldrich, Germany. Other chemicals (pure or of higher purity) used as standards were supplied by Fluka, Aldrich or Merck-Schuchardt. All solvents of trace analysis quality or gradient grade were purchased from Chromservis (Czech Republic).

Organisms and cultivation

The ligninolytic fungal strains Irpex lacteus 617/93,

Results and discussion

As mentioned above, the applied concentrations of the tested EDCs varied in some cases due to their significant toxic effects. Especially NPs suppressed the growth of the fungi already at concentrations of about 5 mg L−1 and TRC at 3 mg L−1 (data not shown). The comparison of EDC estrogenic activity showed that EE2 was 1.5-fold more potent then E2. That corresponds to results of Anderson et al. (1999). All the other compounds were of approximately equal potency with 106 lower activity than E2.

The

Conclusions

In this study, we investigated the abilities of eight ligninolytic fungal strains to degrade several typical representatives of EDCs and a bacteriocide, Trc. Attention was also paid to the effect of EDCs on ligninolytic enzyme activities, and changes in estrogenic activity of the samples during biodegradation were also evaluated. The results discussed above show that almost all the fungi were able to degrade the tested EDCs under the used conditions. I .lacteus and P. ostreatus in particular

Acknowledgements

This work was funded by Grants Nos. LC06066 and 2B06156 of the Ministry of Education, Youth and Sport of the Czech Republic, by Grant KJB600200613 of the Grant Agency of the Academy of Science of the Czech Republic; and also by Institutional Research Concept No. AV0Z50200510.

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